Temporal coordination of tissue transformation, olfactory sensory neural development and central axon projections through morphogens

Abstract

During development, sensory neurons arise in the peripheral sensory organ in close spatial and temporal coordination with the dynamic morphological transformation of the sensory organ in the central nervous system. Moreover, intricate coordination exists between the peripheral map and the central map. Yet, it remains largely unclear what mechanisms are responsible for orchestrating such coordination and whether these mechanisms might be evolutionarily conserved. Here, we performed a systematic analysis of the sensory organ transformation process, defining the expression patterns of morphogens and their receptors at multiple developmental stages and creating receptor mutants in sensory neurons and projections. These experiments revealed combinatorial codes of morphogens that are utilized to coordinate sensory circuit development. Remarkably, two distinct strategies were likely deployed by different morphogen families, including a two-step strategy (same ligand from different sources at two different stages) and a ligand switch strategy (different ligands at two different stages). Significance StatementTissue transformation, dissociation and integration occur in all species. However, it remains largely unclear how such transformations are coordinated with cell fate determination, local cell migration and axonal guidance both temporally and spatially. We found Drosophila antennal discs undergo a series of tissue transformation steps to develop a three-dimensional structure from a two-dimensional neuroepithelium. During this tissue transformation, olfactory sensory neurons acquire their distinct cell types and project their axons to specific targets in the antennal lobe. The whole process is temporally and spatially coordinated by combinatorial codes of morphogens.